Abstract
Phytoplankton biomass–nutrient relationship is widely used by lake managers to assess the eutrophication impact and to set the nutrient targets. Submerged vegetation and large zooplankton grazing have long been identified as factors weakening the relationship by decoupling phytoplankton from nutrients. Proving this decoupling unambiguously is difficult because, in natural systems, many factors act together, blurring each other’s effect. In this article, we present the results of continuous monitoring of 13 ponds where the effects of submerged vegetation and zooplankton grazing were enhanced by biomanipulation (fish removal). The monitoring allowed these effects to be assessed and compared with the pre-biomanipulation situations when phytoplankton biomass was mainly nutrient driven. The comparison showed a strong weakening effect of submerged vegetation and large zooplankton grazing on the chlorophyll a–total phosphorus relationship suggesting that a considerable degree of ecological quality of ponds affected by eutrophication can be restored even when nutrient-loading reduction is not feasible.
Similar content being viewed by others
References
APHA-AWWA-WEF, 1995. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DC.
Benndorf, J., B. Wissel, A. F. Sell, U. Hornig, P. Ritter & W. Böing, 2000. Food web manipulation by extreme enhancement of piscivory: an invertebrate predator compensates for the effects of planktivorous fish on a plankton community. Limnologica – Ecology and Management of Inland Waters 30: 235–245.
Benndorf, J., W. Boing, J. Koop & I. Neubauer, 2002. Top-down control of phytoplankton: the role of time scale, lake depth and trophic state. Freshwater Biology 47: 2282–2295.
Brabrand, A., B. A. Faafeng & J. P. M. Nilssen, 1990. Relative importance of phosphorus supply to phytoplankton production – fish excretion versus external loading. Canadian Journal of Fisheries and Aquatic Sciences 47: 364–372.
Breukelaar, A. W., E. Lammens, J. Breteler & I. Tatrai, 1994. Effects of benthivorous bream (Abramis brama) and carp (Cyprinus carpio) on sediment resuspension and concentrations of nutrients and chlorophyll-a. Freshwater Biology 32: 113–121.
Bronmark, C. & L.-A. Hansson, 2005. The Biology of Lakes and Ponds. Oxford University Press, Oxford.
Burns, C. W., 1968. Relationship between body size of filter-feeding Cladocera and maximum size of particle ingested. Limnology and Oceanography 13: 675–678.
Carpenter, S. R. & J. F. Kitchell, 1992. Trophic cascade and biomanipulation – interface of research and management – Reply. Limnology and Oceanography 37: 208–213.
Carpenter, S. R., J. F. Kitchell & J. R. Hodgson, 1985. Cascading trophic interactions and lake productivity. Bioscience 35: 634–639.
Carpenter, S. R., J. J. Cole, J. R. Hodgson, J. F. Kitchell, M. L. Pace, D. Bade, K. L. Cottingham, T. E. Essington, J. N. Houser & D. E. Schindler, 2001. Trophic cascades, nutrients, and lake productivity: whole-lake experiments. Ecological Monographs 71: 163–186.
Cottingham, K. L. & D. E. Schindler, 2000. Effects of grazer community structure on phytoplankton response to nutrient pulses. Ecology 81: 183–200.
DeMelo, R., R. France & D. J. McQueen, 1992. Biomanipulation – hit or myth. Limnology and Oceanography 37: 192–207.
Dillon, P. J. & F. H. Rigler, 1974. Phosphorus–chlorophyll relationship in lakes. Limnology and Oceanography 19: 767–773.
Dokulil, M. T. & K. Teubner, 2003. Eutrophication and restoration of shallow lakes – the concept of stable equilibria revisited. Hydrobiologia 506: 29–35.
Gliwicz, Z. M., 1990a. Food thresholds and body size in cladocerans. Nature 343: 638–640.
Gliwicz, Z. M., 1990b. Why do cladocerans fail to control algal blooms? Hydrobiologia 200: 83–97.
Gragnani, A., M. Scheffer & S. Rinaldi, 1999. Top-down control of cyanobacteria: a theoretical analysis. American Naturalist 153: 59–72.
Hansson, L. A. & S. R. Carpenter, 1993. Relative importance of nutrient availability and food-chain for size and community composition in phytoplankton. Oikos 67: 257–263.
Hosper, H. & M. L. Meijer, 1993. Biomanipulation, will it work for your lake – a simple test for the assessment of chances for clear water, following drastic fish-stock reduction in shallow, eutrophic lakes. Ecological Engineering 2: 63–72.
Hudnell, H. K., 2008. Cyanobacterial Harmful Algal Blooms – State of the Science and Research Needs. Springer Science, New York.
Irfanullah, H. M. & B. Moss, 2005. A filamentous green algae-dominated temperate shallow lake: variations on the theme of clearwater stable states? Archiv Fur Hydrobiologie 163: 25–47.
Jeppesen, E., J. P. Jensen, M. Sondergaard, T. Lauridsen, L. J. Pedersen & L. Jensen, 1997. Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia 342: 151–164.
Jeppesen, E., M. Sondergaard, J. P. Jensen, K. E. Havens, O. Anneville, L. Carvalho, M. F. Coveney, R. Deneke, M. T. Dokulil, B. O. B. Foy, D. Gerdeaux, S. E. Hampton, S. Hilt, K. Kangur, J. A. N. Kohler, E. H. H. R. Lammens, T. L. Lauridsen, M. Manca, M. R. Miracle, B. Moss, P. Noges, G. Persson, G. Phillips, R. O. B. Portielje, S. Romo, C. L. Schelske, D. Straile, I. Tatrai, E. V. A. Willen & M. Winder, 2005. Lake responses to reduced nutrient loading – an analysis of contemporary long-term data from 35 case studies. Freshwater Biology 50: 1747–1771.
Lammens, E., 1999. The central role of fish in lake restoration and management. Hydrobiologia 396: 191–198.
Lammens, E., R. D. Gulati, M. L. Meijer & E. Vandonk, 1990. The 1st biomanipulation conference – a synthesis. Hydrobiologia 200: 619–627.
Mazumder, A., 1994. Phosphorus chlorophyll relationships under contrasting herbivory and thermal stratification – predictions and patterns. Canadian Journal of Fisheries and Aquatic Sciences 51: 390–400.
Mazumder, A. & K. E. Havens, 1998. Nutrient–chlorophyll–Secchi relationships under contrasting grazer communities of temperate versus subtropical lakes. Canadian Journal of Fisheries and Aquatic Sciences 55: 1652–1662.
Meijer, M. L., I. de Boois, M. Scheffer, R. Portielje & H. Hosper, 1999. Biomanipulation in shallow lakes in The Netherlands: an evaluation of 18 case studies. Hydrobiologia 408: 13–30.
Moss, B., J. Stansfield, K. Irvine, M. Perrow & G. Phillips, 1996. Progressive restoration of a shallow lake: a 12-year experiment in isolation, sediment removal and biomanipulation. Journal of Applied Ecology 33: 71–86.
Moss, B., D. Stephen, C. Alvarez, E. Becares, W. Van de Bund, S. E. Collings, E. Van Donk, E. De Eyto, T. Feldmann, C. Fernandez-Alaez, M. Fernandez-Alaez, R. J. M. Franken, F. Garcia-Criado, E. M. Gross, M. Gyllstrom, L. A. Hansson, K. Irvine, A. Jarvalt, J. P. Jensen, E. Jeppesen, T. Kairesalo, R. Kornijow, T. Krause, H. Kunnap, A. Laas, E. Lille, B. Lorens, H. Luup, M. R. Miracle, P. Noges, T. Noges, M. Nykanen, I. Ott, W. Peczula, E. Peeters, G. Phillips, S. Romo, V. Russell, J. Salujoe, M. Scheffer, K. Siewertsen, H. Smal, C. Tesch, H. Timm, L. Tuvikene, I. Tonno, T. Virro, E. Vicente & D. Wilson, 2003. The determination of ecological status in shallow lakes – a tested system (ECOFRAME) for implementation of the European Water Framework Directive. Aquatic Conservation: Marine and Freshwater Ecosystems 13: 507–549.
Paerl, H. W., 1988. Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnology and Oceanography 33: 823–847.
Peretyatko, A., S. Teissier, S. De Backer & L. Triest, 2011. Biomanipulation of hypereutrophic ponds: when it works and why it fails. Environmental Monitoring and Assessment. doi:10.1007/s10661-011-2057-z.
Peretyatko, A., J.-J. Symoens & L. Triest, 2007a. Impact of macrophytes on phytoplankton in eutrophic peri-urban ponds, implications for pond management and restoration. Belgian Journal of Botany 140: 83–99.
Peretyatko, A., S. Teissier, J.-J. Symoens & L. Triest, 2007b. Phytoplankton biomass and environmental factors over a gradient of clear to turbid peri-urban ponds. Aquatic Conservation: Marine and Freshwater Ecosystems 17: 584–601.
Peretyatko, A., S. Teissier, S. De Backer & L. Triest, 2009. Restoration potential of biomanipulation for eutrophic peri-urban ponds: the role of zooplankton size and submerged macrophyte cover. Hydrobiologia 634: 125–135.
Peretyatko, A., S. Teissier, S. De Backer & L. Triest, 2010. Assessment of the risk of cyanobacterial bloom occurrence in urban ponds: probabilistic approach. Annales De Limnologie – International Journal of Limnology 46: 121–133.
Perrow, M. R., M. L. Meijer, P. Dawidowicz & H. Coops, 1997. Biomanipulation in the shallow lakes: state of the art. Hydrobiologia 342: 355–365.
Phillips, G., O. P. Pietilainen, L. Carvalho, A. Solimini, A. L. Solheim & A. C. Cardoso, 2008. Chlorophyll–nutrient relationships of different lake types using a large European dataset. Aquatic Ecology 42: 213–226.
Pinel-Alloul, B., 1995. Impacts des prédateurs invertébrés sur les communautés aquatiques. In Pourriot, R. & M. Meybeck (eds), Limnologie Générale. Masson, Paris: 628–686.
Pourriot, R., 1995. Réponses adaptatives du zooplancton à la prédation. In Pourriot, R. & M. Meybeck (eds), Limnologie Générale. Masson, Paris: 610–627.
Reynolds, C. S., 1998. What factors influence the species composition of phytoplankton in lakes of different trophic status? Hydrobiologia 369: 11–26.
Reynolds, C. S., 2006. Ecology of Phytoplankton. Cambridge University Press, Cambridge.
Sarnelle, O., 1992. Nutrient enrichment and grazer effects on phytoplankton in lakes. Ecology 73: 551–560.
Scheffer, M., 1998. Ecology of Shallow Lakes. Kluwer Academic Publishers, Dordrecht.
Scheffer, M., S. Carpenter, J. A. Foley, C. Folke & B. Walker, 2001. Catastrophic shifts in ecosystems. Nature 413: 591–596.
Shapiro, J., 1990. Biomanipulation: the next phase – making it stable. Hydrobiologia 200–201: 13–27.
Sierp, M. T., J. G. Qin & F. Recknagel, 2009. Biomanipulation: a review of biological control measures in eutrophic waters and the potential for Murray cod Maccullochella peelii peelii to promote water quality in temperate Australia. Reviews in Fish Biology and Fisheries 19: 143–165.
Sondergaard, M. & B. Moss, 1998. Impact of submerged macrophytes on phytoplankton in shallow freshwater lakes. In Jeppessen, E., M. Sondergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 115–133.
Sondergaard, M., J. P. Jensen & E. Jeppesen, 2005a. Seasonal response of nutrients to reduced phosphorus loading in 12 Danish lakes. Freshwater Biology 50: 1605–1615.
Sondergaard, M., E. Jeppesen & J. P. Jensen, 2005b. Pond or lake: does it make any difference? Archiv Fur Hydrobiologie 162: 143–165.
Steiner, C. F., 2002. Context-dependent effects of Daphnia pulex on pond ecosystem function: observational and experimental evidence. Oecologia 131: 549–558.
Sterner, R. W., J. J. Elser & D. O. Hessen, 1992. Stoichiometric relationships among producers, consumers and nutrient cycling in pelagic ecosystems. Biogeochemistry 17: 49–67.
United Nations Environment Programme, 2003. Planning and Management of Lakes and Reservoirs: An Integrated Approach to Eutrophication. UNEP Newsletter.
van Donk, E. & W. J. van de Bund, 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72: 261–274.
Vanni, M. J., 2002. Nutrient cycling by animals in freshwater ecosystems. Annual Review of Ecology and Systematics 33: 341–370.
Acknowledgements
This study was supported by the Prospective Research for Brussels (2003–2006), the Research in Brussels (2006), the Belgian Science Policy (project BBlooms 2: Cyanobacterial blooms: toxicity, diversity, modelling and management, contract SD/TE/01A) and Brussels Institute of Environment (BIM/IBGE). We thank the two anonymous reviewers for their valuable comments that helped us improve the manuscript substantially.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: D. Boix, B. Oertli, R. Céréghino, T. Kalettka, J. Biggs & A. P. Hull / Pond Research and Management in Europe – Proceedings of the 4th conference of the European Pond Conservation Network (Berlin 2010)
Rights and permissions
About this article
Cite this article
Teissier, S., Peretyatko, A., De Backer, S. et al. Strength of phytoplankton–nutrient relationship: evidence from 13 biomanipulated ponds. Hydrobiologia 689, 147–159 (2012). https://doi.org/10.1007/s10750-011-0726-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-011-0726-0